What's So Special about Human Tool Use?

Scott H Johnson-Frey
2003 Neuron  
Dartmouth College and transforming a representation of objects' extrinsic spa-Department of Psychiatry tial properties (i.e., location, orientation) and knowledge Dartmouth Medical School of the limb's position into a motor plan. In macaques, Hanover, New Hampshire 03755 these transformations are accomplished within a circuit interconnecting one or more regions located within the medial intraparietal sulcus (IPS) and dorsal premotor Evidence suggests homologies in parietofrontal circortex (PMd)
more » ... (Andersen and Buneo, 2002; Johnson et cuits involved in object prehension among humans al. , 1996). Area PMd is well situated for computing preand monkeys. Likewise, tool use is known to induce movement plans for reaching. It receives direct visual functional reorganization of their visuotactile limb repand higher-level proprioceptive input from the superior resentations. Yet, humans are the only species for parietal lobule (SPL). Likewise, somatosensory informawhom tool use is a defining and universal characteristion concerning limb position is provided to PMd via a tic. Why? Comparative studies of chimpanzee tool use circuit interconnecting PEc/PEip-F2. This sensory input indicate that critical differences are likely to be found is integrated within PMd neurons to form plans for using in mechanisms involved in causal reasoning rather a particular limb to reach to a specific target location than those implementing sensorimotor transforma-(Hoshi and Tanji, 2000). Evidence for a "reach" circuit tions. Available evidence implicates higher-level perin humans involving putative homologs of medial intraceptual areas in these processes. parietal cortex and PMd has recently been reported (Johnson et al., 2002). Interacting manually with objects in the environment Grasp System. Grasping involves integrating repreposes considerable challenges for the sensorimotor sentations of objects' intrinsic spatial properties (e.g., systems of primates. Electrophysiological studies of shape, size, texture) with properties of the hand and nonhuman primates suggest that these problems are fingers. In the macaques, this is accomplished in a more solved by functionally specialized parietofrontal circuits ventral parietofrontal circuit connecting the anterior inthat transform sensory representations of the body and traparietal area (AIP) and area F5 located in ventral prethe surrounding environment into motor plans for premotor cortex (PMv) (Sakata et al., 1997) . Area AIP conhension (reaching, grasping, and manipulation of obtains several subpopulations of "manipulation" cells that jects). The efficiency of these solutions is attested to by represent specific types of hand postures necessary for the universality of dexterous prehension among prigrasping objects of differing shapes. Area F5ab receives mates. a major projection from AIP, and cells appear to repre-Tool use introduces a new set of difficulties. The physsent specific manual actions (Rizzolatti et al., 2002). In ical characteristics of the tool, its relationship to the humans, significant activation within the anterior IPS body and to the surrounding environment all impinge (putative AIP) and inferior frontal cortex is observed upon its effective utilization. While many species dexter when objects are grasped (Binkofski et al., 1999), and lesions in this circuit produce deficits in configuring the ously use simple tools to solve problems in their environhand to engage objects effectively (Binkofski et al., ments, the ability of even our closest living relative, the 1998). chimpanzee, to solve environmental challenges through Manipulation System. Visuotactile representations of tool use pales in comparison to that of young children. peripersonal space centered on the body part involved With growing evidence for homologies among primates in a given visually guided action, such as object manipuin parietofrontal circuits that control prehension, the oblation, are constructed in a circuit connecting the ventral vious question is why? intraparietal area (VIP) with area F4 in PMv (Graziano Homologous Parietofrontal Systems and Gross, 1998) (Figure 1). The majority of units in F4 for Prehension are bimodal, having tactile receptive fields (RFs) that As summarized in Figure 1, electrophysiological studies are in register with 3D visual RFs of space immediately of macaques reveal the existence of parietofrontal ciradjacent to the animal. Similar RF properties are found cuits that are involved in sensory-guided prehension. in VIP and in cells distributed throughout the IPS. What The precise computations implemented within these ciris special about these units is that their receptive field cuits are a source of ongoing research and debate that properties are altered by tool use. Specifically, as shown exceed the scope of this review (see Andersen and Buin Figure 2, visual RFs expand when monkeys use a rake neo, 2002; Marconi et al., 2001; Rizzolatti and Luppino, to retrieve other objects (i.e., food pellets; Iriki et al., 2001). Nevertheless, parietofrontal circuits involved in 1996) . Visual RFs normally in register with tactile RFs of reaching, grasping, and object manipulation have been the hand now encompass peripersonal space occupied distinguished, and a growing body of evidence from by the rake. Importantly, such expansion is not observed functional neuroimaging points to the existence of howhen monkeys unsuccessfully attempt to retrieve food with an ineffective manipulandum (Figure 2) . Therefore the increase in the representation of peripersonal space *Correspondence: scott.h.johnson@dartmouth.edu Neuron 202
doi:10.1016/s0896-6273(03)00424-0 pmid:12873378 fatcat:q6qf27jixbctlayjpaizbrn5e4